Journal of Applied Phycology

, Volume 29, Issue 5, pp 2377–2398 | Cite as

Consumption of seaweeds and the human brain

  • M. Lynn Cornish
  • Alan T. Critchley
  • Ole G. Mouritsen
22ND INTERNATIONAL SEAWEED SYMPOSIUM, COPENHAGEN

Abstract

Much of the content of the human head is brain matter. This functions as the epicenter of human physical existence, including a sense of well-being and the manifestation of human consciousness. The human brain is a precious and complex organ which increases from 350 to 400 g in infants to 1.3–1.4 kg in adults; it comprises ca. 78 % water, 12 % lipid, 8 % protein, and 1 % carbohydrate. Significant progress in behavioral and analytical science has accelerated understanding of the multifaceted responses of the brain to stimuli, whether it be the microbial breakdown products of ingested foods, the influences of environment, or in relation to genetic predisposition. The science of seaweeds, and particularly their broad range of applications, is gathering momentum as studies repeatedly underscore the natural health and nutritional benefits of dietary macroalgae. This article reviews research highlighting the potential impacts of the consumption of a variety of seaweeds on human brain health and includes theories in relation to the benefits to early Homo sapiens. The emphasis is on a varied diet including macroalgae and the gut/microbe/brain axis, the importance of polyunsaturated fatty acids, and the impacts of anti-oxidant activities in neuroprotection. These elements have the capacity to help in the defense of human cognitive disorders, such as dementia, Alzheimer’s disease, depression, bipolar diseases, and adverse conditions characterized by progressive neurodegeneration. Psychological benefits associated with the moderate consumption of a diet fortified with macroalgae are also discussed in terms of reduction of depressive symptoms and furthermore highlighting possible improvements in sexual function.

Keywords

Seaweeds Food Essential nutrients Micronutrients Brain development Neural system Neural diseases Polyunsaturated fatty acids Taurine Magnesium Zinc Vitamin B12 Iodine Antioxidants 

References

  1. Ahn BR, Moon HE, Kim HR, Jung HA, Choi JS (2012) Neuroprotective effect of edible brown alga Eisenia bicyclis on amyloid beta peptide-induced toxicity in PC12 cells. Arch Pharm Res 35:1989–1998PubMedCrossRefGoogle Scholar
  2. Aiello LC, Wheeler P (1995) The expensive tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221CrossRefGoogle Scholar
  3. Al MDM, Hornstra G, van der Schouw YT, Bulstra-Ramakers MTEW, Huisjes HJ (1990) Biochemical EFA status of mothers and their neonates after normal pregnancy. Early Human Dev 24:239–248CrossRefGoogle Scholar
  4. Al MDM, van Houwelingen AC, Kester AD, Hasaart TH, de Jong AE, Hornstra G (1995) Maternal essential fatty acid patterns during normal pregnancy and their relationship to the neonatal essential fatty acid status. Br J Nutr 74:55–68PubMedCrossRefGoogle Scholar
  5. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S (2012) Gut microbial communities modulating brain development and function. Gut Microbes 3:366–373PubMedPubMedCentralCrossRefGoogle Scholar
  6. Alghazwi M, Kan YQ, Zhang W, Gai WP, Garson MJ, Smid S (2016) Neuroprotective activities of natural products from marine macroalgae during 1999-2015. J Appl Phycol 28:3599–3616CrossRefGoogle Scholar
  7. Allman JM (2000) Evolving brains. Library of Congress Cataloguing. ISBN 0-7167-5076-7. Scientific American Library, New YorkGoogle Scholar
  8. Anantharaman P, Karthikaidevi G, Manivannan K, Thirumaran G, Balasubramanian T (2010) Mineral composition of marine macroalgae from Mandapam coastal regions; southeast coast of India. Recent Res Sci Technol 2:66–71Google Scholar
  9. Antonow-Schlorke I, Schwab M, Cox LA, Li C, Stuchlik K, Witte OW, Nathanielsz PW, McDonald TJ (2011) Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. PNAS 108:3011–3016PubMedPubMedCentralCrossRefGoogle Scholar
  10. Astorga-España MS, Calisto-Ulloa NC, Guerrero S (2007) Baseline concentrations of trace metals in macroalgae from the Strait of Magellan, Chile. Bull Environ Contam Toxicol 80:97–101PubMedCrossRefGoogle Scholar
  11. Bae YJ, Bu SY, Kim JY, Yeon JY, Sohn EW, Jang KH, Lee JC, Kim MH (2011) Magnesium supplementation through seaweed calcium extract rather than synthetic magnesium oxide improves femur bone density and strength in ovariectomized rats. Biol Trace Elem Res 144:992–1002PubMedCrossRefGoogle Scholar
  12. Barbosa M, Valentão P, Andrade PB (2014) Bioactive compounds from macroalgae in the new millennium: implications for neurodegenerative diseases. Mar Drugs 12:4934–4972PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bath SC, Steer CD, Golding J, Emmett P, Rayman MP (2013) Effect of inadequate iodine status in UK pregnant women on cognitive outcomes in their children: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Lancet 382:331–337PubMedCrossRefGoogle Scholar
  14. Bazan NG, Molina MF, Gordon WC (2011) Docosahexaenoic acid signalolipodomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer’s and other neurodegenerative diseases. Annu Rev Nutr 31:321–351PubMedPubMedCentralCrossRefGoogle Scholar
  15. Beaumetz D (1885) Clinical therapeutics: the treatment of nervous diseases, of general diseases, and of fevers. George E. Davis, DetroitGoogle Scholar
  16. Berthoud HR (2008) Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterol Motil (Suppl. 1):64–72Google Scholar
  17. Bhuiyan MMH, Mohibbullah M, Hannan MA, Hong YK, Choi JS, Choi IS, Moon IS (2015) Undaria pinnatifida promotes spinogenesis and synaptogenesis and potentiates functional presynaptic plasticity in hippocampal neurons. Am J Chin Med 43:529–542CrossRefGoogle Scholar
  18. Birch EE, Garfield S, Castañeda Y, Hughbanks-Wheaton D, Uauy R, Hoffman D (2007) Visual acuity and cognitive outcomes at 4 years of age in a double-blind, randomized trial of long-chain polyunsaturated fatty acid-supplemented infant formula. Early Hum Dev 83:279–284PubMedCrossRefGoogle Scholar
  19. Blekhman R, Oshlack A, Chabot AE, Smyth GK, Gilad Y (2008) Gene regulation in primates evolves under tissue specific selection pressures. PLoS Genet 4:e1000271PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bonnaventura P, Benedetti G, Albarède F, Miossec P (2015) Zinc and its role in immunity and inflammation. Autoimmun Rev 14:277–285CrossRefGoogle Scholar
  21. Bourre JM (2006) Effects of nutrients (in food) on the structure and function of the nervous system: update on dietary requirements for brain. Part 1: micronutrients. J Nutr Health Age 10:377–385Google Scholar
  22. Bouwstra H, Dijck-Brouwer J, Decsi T, Boehm G, Boersma ER, Muskiet FAJ, Hadders-Algra M (2006) Neurologic condition of healthy term infants at 18 months: positive association with venous umbilical DHA status and negative association with umbilical trans-fatty acids. Pediatr Res 60:334–339PubMedCrossRefGoogle Scholar
  23. Brenna JT, Carlson SE (2014) Docosahexaenoic acid and human brain development: evidence that a dietary supply is needed for optimal development. J Human Evol 77:99–106CrossRefGoogle Scholar
  24. Briani C, Torre CD, Citton V, Manara R, Pompanin S, Binotto G, Adami F (2013) Cobalamin deficiency: clinical picture and radiological findings. Nutrients 5:4521–4539PubMedPubMedCentralCrossRefGoogle Scholar
  25. Broberg A, Kenne L, Pedersén M (1998) In-situ identification of major metabolites in the red alga Gracilariopsis lemaneiformis using high-resolution magic angle spinning nuclear magnetic resonance spectroscopy. Planta 206:300–307CrossRefGoogle Scholar
  26. Bumsted MP (1981) The potential of stable carbon isotopes in bioarcheological anthropology. Research Report 20: Biocultural Adaptation Comprehensive Approaches to Skeletal Analysis. Paper 12. http://scholarworks.umass.edu/anthro_res_rpt20/12 (Accessed August 10, 2016)
  27. Burri L, Hoem N, Banni S, Berge K (2012) Marine omega-3 phospholipids: metabolism and biological activities. Int J Mol Sci 13:15401–15419PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150CrossRefGoogle Scholar
  29. Camp JG, Kanther M, Semova I, Rawls JF (2009) Patterns and scales in gastrointestinal microbial ecology. Gastroenterol 136:1989–2002CrossRefGoogle Scholar
  30. Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, Kim HY (2009) Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem 111:510–521PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cerling TE, Manthi FK, Mbua EN, Leakey LN, Leakey MG, Leakey RE, Brown FH, Grine FE, Hart JA, Kaleme P, Roche H, Uno KT, Wood BA (2013) Stable isotope-based diet reconstructions of Turkana Basin hominins. PNAS 110:10501–10506PubMedPubMedCentralCrossRefGoogle Scholar
  32. Chance R, Baker AR, Küpper FC, Hughes C, Kloareg B, Malin G (2009) Release and transformations of inorganic iodine by marine macroalgae. Estuar Coast Shelf Sci 82:406–414CrossRefGoogle Scholar
  33. Charoensiddhi S, Conlon MA, Vuaran MS, Franco CMM, Zhang W (2016) Impact of extraction processes on prebiotic potential of the brown seaweed Ecklonia radiata by in vitro human gut bacteria fermentation. J Funct Foods 24:221–230CrossRefGoogle Scholar
  34. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME (2012) Zinc and human health: an update. Arch Toxicol 86:521–534PubMedCrossRefGoogle Scholar
  35. Chen WQ, Jin H, Nguyen M, Carr J, Lee YJ, Hsu CC, Faiman MD, Schloss JV, Wu JY (2001) Role of taurine in regulation of intracellular calcium level and neuroprotective function in cultured neurons. J Neurosci Res 66:612–619PubMedCrossRefGoogle Scholar
  36. Chen CT, Liu Z, Ouellet M, Calon F, Bazinet RP (2009) Rapid β-oxidation of eicosapentaenoic acid in mouse brain: an in situ study. Prosta Leuko Essent Fatty Acids 80:157–163CrossRefGoogle Scholar
  37. Chen CT, Liu Z, Bozinet RP (2011) Rapid de-esterfication and loss of eicosapentaenoic acid from rat brain phospholipids: an intracerebroventricular study. J Neurochem 116:363–373PubMedCrossRefGoogle Scholar
  38. Chen S, Zhang H, Pu H, Wang G, Li W, Leak RK, Chen J, Liou AK, Hu X (2014) n-3 PUFA supplementation benefits microglial responses to myelin pathology. Sci Rep 4:7458PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chhetry BT, Hezghia A, Miller JM, Lee S, Rubin-Falcon H, Cooper TB, Oquendo MA, Mann JJ, Sublette ME (2016) Omega-3 polyunsaturated fatty acid supplementation and white matter changes in major depression. J Psych Res 75:65–74CrossRefGoogle Scholar
  40. Chojnacka K, Saeid A, Witkowska Z, Tuhy L (2012) Biologically active compounds in seaweed extracts—the prospects for the application. The Open Conf J 3(Suppl-M4):20–28CrossRefGoogle Scholar
  41. Cian RE, Drago SR, Sánchez de Medina F, Martínez-Augustin O (2015) Proteins and carbohydrates from red seaweeds: evidence for beneficial effects on gut function and microbiota. Mar Drugs 13:5358–5383PubMedPubMedCentralCrossRefGoogle Scholar
  42. Clandinin MT, Chappell JE, Leong S, Heim T, Swyer PR, Chance GW (1980) Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Human Dev 4:121–129CrossRefGoogle Scholar
  43. Collingridge GL, Volianskis A, Bannister N, France G, Hanna L, Mercier M, Tidball P, Fang G, Irvine MW, Costa BM, Monaghan DT, Bortolotto ZA, Molnár E, Lodge D, Jane DE (2013) The NMDA receptor as a target for cognitive enhancement. Neuropharm 64:13–26CrossRefGoogle Scholar
  44. Combet E, Ma ZF, Cousins F, Thompson B, Lean MEJ (2014) Low-level seaweed supplementation improves iodine status in iodine-insufficient women. Br J Nutr 112:753–761PubMedCrossRefGoogle Scholar
  45. Cornish ML, Garbary DJ (2010) Antioxidants from macroalgae: potential applications in human health and nutrition. Algae 25:155–171CrossRefGoogle Scholar
  46. Cornish ML, Critchley AT, Mouritsen OG (2015) A role for dietary macroalgae in the amelioration of certain risk factors associated with cardiovascular disease. Phycologia 54:649–666CrossRefGoogle Scholar
  47. Crawford MA (1992) The role of dietary fatty acids in biology: their place in the evolution of the human brain. Nutr Rev 50:3–11PubMedCrossRefGoogle Scholar
  48. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93PubMedCrossRefGoogle Scholar
  49. Croft MT, Warren MJ, Smith AG (2006) Algae need their vitamins. Eukar Cell 5:1175–1183CrossRefGoogle Scholar
  50. Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Neuroscience 13:701–712PubMedGoogle Scholar
  51. Cunnane SC, Crawford MA (2014) Energetic and nutritional constraints on infant brain development: implications for brain expansion during human evolution. J Human Evol 77:88–98CrossRefGoogle Scholar
  52. Custódio L, Silvestre L, Rocha MI, Rodrigues MJ, Vizetto-Duarte C, Pereira H, Barreira L, Varela J (2015) Methanol extracts from Cystoseira tamariscifolia and Cystoseira nodicaulis are able to inhibit cholinesterases and protect a human dopaminergic cell line from hydrogen peroxide-induced cytotoxicity. Pharma Biol. doi:10.3109/13880209.2015.1123278 Google Scholar
  53. Cutuli D, De Bartolo P, Caporali P, Laricchiuta D, Foti F, Ronci M, Rossi C, Neri C, Spalletta G, Caltagirone C, Farioli-Vecchioli S, Petrosini L (2014) n-3 polyunsaturated fatty acid supplementation enhances hippocampal functionality in aged mice. Front Aging Neurosci 6:220PubMedPubMedCentralCrossRefGoogle Scholar
  54. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899CrossRefGoogle Scholar
  55. De Clerck O, Bogaert KA, Leliaert F (2012) Diversity and evolution of algae: primary endosymbiosis. Adv Bot Res 64:56–86Google Scholar
  56. Deoni SC, Mercure E, Blasi A, Gasston D, Thomson A, Johnson M, Williams SC, Murphy DG (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784–791PubMedCrossRefGoogle Scholar
  57. Deoni SC, Dean DC 3rd, O’Muircheartaigh J, Dirks H, Jerskey BA (2012) Investigating white matter development in infancy and early childhood using myelin water faction and relaxation time mapping. NeuroImage 63:1038–1053PubMedPubMedCentralCrossRefGoogle Scholar
  58. Dietitians of Canada (2014) Minerals. http://www.dietitions.ca/Your-Health/Nutrition-A-Z/Minerals.aspx (Accessed August 10, 2016)
  59. Dijck-Brouwer DAJ, Hadders-Algra M, Bouwstra H, Decsi T, Boehm G, Martini IA, Boersma ER, Muskiet FAJ (2005) Lower fetal status of docosahexaenoic acid, arachidonic acid and essential fatty acids is associated with less favorable neonatal neurological condition. Prostoglan Leuko Essent FA 72:21–28CrossRefGoogle Scholar
  60. Dillehay TD, Ramírez C, Pino M, Collins MB, Rossen J, Pino-Navarro JD (2008) Monte Verde: seaweed, food, medicine, and the peopling of South America. Science 320:784–786PubMedCrossRefGoogle Scholar
  61. Dinan TG, Stilling RM, Stanton C, Cryan JF (2015) Collective unconscious: how gut microbes shape human behavior. J Psych Res 63:1–9CrossRefGoogle Scholar
  62. Dominy J Jr, Thinschmidt JS, Peris J, Dawson R Jr, Papke RL (2004) Taurine-induced long-lasting potentiation in the rat hippocampus shows a partial dissociation from total hippocampal taurine content and independence from activation of known taurine transporters. J Neurochem 89:1195–1205PubMedCrossRefGoogle Scholar
  63. Dror DK, Allen LH (2008) Effect of vitamin B12 deficiency on neurodevelopment in infants: current knowledge and possible mechanisms. Nutr Rev 66:250–255PubMedCrossRefGoogle Scholar
  64. Emken EA, Adolf RO, Gulley RM (1994) Dietary linoleic acid influences desaturation and acylation of deuterium-labeled linoleic and linolenic acids in young adult males. Biochim Biophys Acta 1213:277–288PubMedCrossRefGoogle Scholar
  65. Erlandson JM, Moss ML (2015) Shellfish feeders, carrion eaters, and the archeology of aquatic adaptations. Amer Antiquity 66:413–432CrossRefGoogle Scholar
  66. Ezatti M, Lopez AD, Rodgers A, Hoorn SV, Murray CLJ, the Comparative Risk Assessment Collaborating Group (2002) Selected major risk factors and global and regional burden of disease. Lancet 360:1347–1360CrossRefGoogle Scholar
  67. Farquharson J, Cockburn F, Patrick WA, Jamieson EC, Logan RW (1992) Infant cerebral cortex fatty acid composition and diet. Lancet 340:810–813PubMedCrossRefGoogle Scholar
  68. Feifer A, Carrier S (2008) Pharmacotherapy for erectile dysfunction. Expert Opin Investig Drugs 17:679–690PubMedCrossRefGoogle Scholar
  69. Fields RD (2008) White matter matters. Sci Amer 298:54–61CrossRefGoogle Scholar
  70. Fields RD (2011) The other brain. Simon & Schuster, New YorkGoogle Scholar
  71. Forsythe P, Kunze WA (2013) Voices from within: gut microbes and the CNS. Cell Molec Life Sci 70:55–69Google Scholar
  72. Fouhy F, Ross RP, Fitzgerald G, Stanton C, Cotter PD (2012) Composition of the early intestinal microbiota. Gut Microbes 3:203–220PubMedPubMedCentralCrossRefGoogle Scholar
  73. Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB (2000) Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130:1471S–1483SPubMedGoogle Scholar
  74. Froger N, Cadetti L, Lorach H, Martins J, Bemelmans AP, Dubus E, Degardin J, Pain D, Forster V, Chicaud L, Ivkovic I, Simonutti M, Fouquet S, Jammoul F, Léveillard T, Benosman R, Sahel JA, Picaud S (2012) Taurine provides neuroprotection against retinal ganglion cell degeneration. PLoS One 7(10):e42017PubMedPubMedCentralCrossRefGoogle Scholar
  75. Fuster JM (2002) Frontal lobe and cognitive development. J Neurocytol 31:373–385PubMedCrossRefGoogle Scholar
  76. Georgiadis JR, Kringelbach ML (2012) The human sexual response cycle: brain imaging evidence linking sex to other pleasures. Prog Neurobiol 98:49–81PubMedCrossRefGoogle Scholar
  77. Gerster H (1998) Can adults adequately convert α-linolenic acid (18:3 n-3) to eicosapentaenoic acid (20:5 n-3) and docosahexaenoic acid (22:6 n-3)? Int J Vitam Nutr Res 68:159–173PubMedGoogle Scholar
  78. Ghys A, Bakker E, Hornstra G, van den Hout M (2002) Red blood cell and plasma phospholipid arachidonic and docosahexaenoic acid levels at birth and cognitive development at 4 years of age. Ear Human Dev 69:83–90CrossRefGoogle Scholar
  79. Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A, Gareau M, Murphy EF, Saulnier D, Loh G, Macfarlane S, Delzenne N, Ringel Y, Kozianowski G, Dickmann R, Lenoir-Wijnkoop I, Walker C, Buddington R (2010) Dietary prebiotics: current status and new definition. Food Sci Technol Bull Func Foods 7:1–19CrossRefGoogle Scholar
  80. Glazko GV, Nei M (2003) Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20:424–434PubMedCrossRefGoogle Scholar
  81. Gluckman PD, Hanson MA (2004) Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med 9:419–425PubMedCrossRefGoogle Scholar
  82. Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P (2010) Dietary fibre and physicochemical properties of several edible seaweeds from the northwestern Spanish coast. Food Res Inter 43:2289–2294CrossRefGoogle Scholar
  83. Goraya JS, Kaur S, Mehra B (2015) Neurology of nutritional vitamin B12 deficiency in infants: case series from India and literature review. J Child Neurol 30:1831–1837PubMedCrossRefGoogle Scholar
  84. Grayson DS, Kroenke CD, Neuringer M, Fair DA (2014) Dietary omega-3 fatty acids modulate large-scale systems organization in the rhesus macaque brain. J Neurosci 34:2065–2074PubMedPubMedCentralCrossRefGoogle Scholar
  85. Guiry MD, Morrison L (2013) The sustainable harvesting of Ascophyllum nodosum (Fucaceae, Phaeophyceae) in Ireland, with notes on the collection and use of some other brown algae. J Appl Phycol 25:1823–1830CrossRefGoogle Scholar
  86. Gupta L, Gupta RK, Gupta PK, Malhotra HS, Saha I, Garg RK (2016) Assessment of brain cognitive functions in patients with vitamin B12 deficiency using resting state functional MRI: a longitudinal study. Magn Reson Imaging 34:191–196PubMedCrossRefGoogle Scholar
  87. Haag M (2003) Essential fatty acids and the brain. Can J Psychiatr 48:195–203CrossRefGoogle Scholar
  88. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, New YorkGoogle Scholar
  89. Hannan MA, Kang JY, Hong YK, Lee HS, Chowdhury MTH, Choi J-S, Choi IS, Moon IS (2012) A brown alga Sargassum fulvellum facilitates neuronal maturation and synaptogenesis. In Vitro Cell Devel Biol Anim 48:535–544CrossRefGoogle Scholar
  90. Hannan MA, Kang JY, Hong YK, Lee HS, Choi JS, Choi IS, Moon IS (2013) The marine alga Gelidium amansii promotes the development and complexity of neuronal cytoarchitecture. Phytother Res 27:21–29PubMedCrossRefGoogle Scholar
  91. Hannan MA, Mohibbullah M, Hong YK, Nam JH, Moon IS (2014a) Gelidium amansii promotes dendritic spine morphology and synaptogenesis, and modulates NMDA receptor-mediated postsynaptic current. In Vitro Cell Devel Biol Anim 50:445–452CrossRefGoogle Scholar
  92. Hannan MA, Mohibbullah M, Hwang SY, Lee K, Kim YC, Hong YK, Moon IS (2014b) Differential neuritogenic activities of two edible brown macroalgae, Undaria pinnatifida and Saccharina japonica. Am J Chin Med 42:1371–1384PubMedCrossRefGoogle Scholar
  93. Harnedy PA, FitzGerald RJ (2011) Bioactive proteins, peptides, and amino acids from macroalgae. J Phycol 47:218–232PubMedCrossRefGoogle Scholar
  94. Harrison NL, Simmonds MA (1985) Quantitative studies on some antagonists of N-methyl d-aspartate in slices of rat cerebral cortex. Br J Pharmacol 84:381–391PubMedPubMedCentralCrossRefGoogle Scholar
  95. Hartline DK (2008) What is myelin? Neuron Glia Biol 4:153–163PubMedCrossRefGoogle Scholar
  96. Hawks J, Hunley K, Lee S-H, Wolpoff M (2000) Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 17:2–22PubMedCrossRefGoogle Scholar
  97. Haygood R, Fedrigo O, Hanson B, Yokoyama K-D, Wray GA (2007) Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 9:1140–1144CrossRefGoogle Scholar
  98. Health Canada. (2010-1005) Dietary reference intakes. http://www.hc-sc.gc.ca/fn-an/nutrition/reference/table/index-eng.php (Accessed August 10, 2016).
  99. Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–912PubMedCrossRefGoogle Scholar
  100. Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. PNAS 108:3047–3052PubMedCentralCrossRefGoogle Scholar
  101. Heim G, Walsh AM, Sweeney T, Doyle DN, O’Shea CJ, Ryan MT, O’Doherty JV (2014) Effect of seaweed-derived laminarin and fucoidan and zinc oxide on gut morphology, nutrient transporters, nutrient digestibility, growth performance and selected microbial populations in weaned pigs. Brit J Nutr 111:1577–1585PubMedCrossRefGoogle Scholar
  102. Helland IB, Smith L, Saarem K, Saugstad OD, Drevon CA (2003) Maternal supplementation with very long chain n-3 fatty acids during pregnancy and lactation augments children’s IQ at 4 years of age. Pediatrics 111:e39–e44PubMedCrossRefGoogle Scholar
  103. Helliwell KE, Collins S, Kazamia E, Purton S, Wheeler GL, Smith A (2015) Fundamental shift in vitamin B12 ecophysiology of a model alga demonstrated by experimental evolution. ISME J 9:1446–1455PubMedCrossRefGoogle Scholar
  104. Hempel CJ (1880) Materia medica and therapeutics, vol 1. W.A. Chatterton, ChicagoGoogle Scholar
  105. Heo SJ, Cha SH, Kim KN, Lee SH, Ahn G, Kang DH, Oh C, Choi YU, Affan A, Kim D, Jeon YJ (2012) Neuroprotective effect of phlorotannin isolated from Ishige okamurae against H2O2-induced oxidative stress in murine hippocampal neuronal cells, HT22. Appl Biochem Biotechnol 166:1520–1532PubMedCrossRefGoogle Scholar
  106. Hernández-Benítez R, Vanqipuram SD, Ramos-Mandujano G, Lyman WD, Pasantes-Morales H (2013) Taurine enhances the growth of neural precursors derived from fetal human brain and promotes neuronal specification. Dev Neurosci 35:40–49PubMedCrossRefGoogle Scholar
  107. Hibbeln JR (2007) Omega-3 fatty acid deficiencies and the global burden of psychiatric disorders. Biol Skr Dansk Videsk Selsk 56:25–32Google Scholar
  108. Hibbeln JR, Davis JM, Steer C, Emmett P, Rogers I, Williams C, Golding J (2007) Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 369:578–585PubMedCrossRefGoogle Scholar
  109. Hofman MA (2014) Evolution of the human brain: when bigger is better. Front Neuroanat 8:1–12CrossRefGoogle Scholar
  110. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  111. Holloway RL, Sherwood CC, Hof PR, Rilling JK (2009) Evolution of the brain in humans: paleoneurology. In: Encyclopedia of neuroscience. Springer-Verlag, Berlin pp. 1326–1334Google Scholar
  112. Hu P, Li Z, Chen M, Sun Z, Ling Y, Jiang J, Huang C (2016) Structural elucidation and protective role of a polysaccharide from Sargassum fusiforme on ameliorating learning and memory deficiencies in mice. Carbohydr Polym 139:150–158PubMedCrossRefGoogle Scholar
  113. Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163PubMedGoogle Scholar
  114. Jo WK, Zhang Y, Emrich HM, Dietrich DE (2015) Glia in the cytokine-mediated onset of depression: fine tuning the immune response. Front Cell Neurosci 9:268PubMedPubMedCentralCrossRefGoogle Scholar
  115. Jutur PP, Nesamma AA, Shaikh KM (2016) Algae-derived marine oligosaccharides and their biological applications. Front Mar Sci 3:83CrossRefGoogle Scholar
  116. Kadohisa M (2015) Beyond flavor to the gut and back. Flavour 4:37CrossRefGoogle Scholar
  117. Kalappa BI, Anderson CT, Goldberg JM, Lippard SJ, Tzounopoulos T (2015) AMPA receptor inhibition by synaptically released zinc. PNAS 112:15749–15754PubMedPubMedCentralGoogle Scholar
  118. Kang K, Park Y, Hwang HJ, Kim SH, Lee JG, Shin HC (2003) Antioxidative properties of brown algae polyphenolics and their perspectives as chemopreventive agents against vascular risk factors. Arch Pharm Res 26:286–293PubMedCrossRefGoogle Scholar
  119. Kang SM, Cha SH, Ko JY, Kang MC, Kim D, Heo SJ, Kim JS, Heu MS, Kim YT, Jung WK, Jeon YJ (2012) Neuroprotective effects of phlorotannins isolated from a brown alga, Ecklonia cava, against H2O2-induced oxidative stress in murine hippocampal HT22 cells. Envir Toxicol Pharmacol 34:96–105CrossRefGoogle Scholar
  120. Kannan RRR, Aderogba MA, Ndhlala AR, Stirk WA, Van Staden J (2013) Acetylcholinesterase inhibitory activity of phlorotannins isolated from the brown alga, Ecklonia maxima (Osbeck) Papenfuss. Food Res Int 54:1250–1254CrossRefGoogle Scholar
  121. Kazamia E, Czesnick H, Van Nguyen TT, Crodt MT, Sherwood E, Sasso S, Hodson SJ, Warren MJ, Smith AG (2012) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 14:1466–1476PubMedCrossRefGoogle Scholar
  122. Kiecolt-Glaser JK, Derry HM, Fagundes CP (2015) Inflammation: depression fans the flames and feasts on the heat. Am J Psychiatry 172:1075–1091PubMedCrossRefGoogle Scholar
  123. Kim KA, Kim SM, Kang SW, Jeon SI, Um BH, Jung SH (2012) Edible seaweed, Eisenia bicyclis, protects retinal ganglion cells death caused by oxidative stress. Mar Biotech 14:383–395CrossRefGoogle Scholar
  124. Kim M, Li YX, Dewapriya P, Ryu BM, Kim SK (2013) Floridoside suppresses pro-inflammatory responses by blocking MAPK signaling in activated microglia. BMB Rep 46:398–403PubMedPubMedCentralCrossRefGoogle Scholar
  125. Kim IH, Yoo KY, Park JH, Yan BC, Ahn JH, Lee JC, Kwon HM, Kim JD, Kim YM, You SG, Kang IJ, Won MH (2014) Comparison of neuroprotective effects of extract and fractions from Agarum clathratum against experimentally induced transient cerebral ischemic damage. Pharm Biol 52:335–343PubMedCrossRefGoogle Scholar
  126. Kozlowski P, Raj D, Liu J, Lam C, Yung AC, Tetzlaff W (2008) Characterizing white matter damage in rat spinal cord with quantitative MRI and histology. J Neurotraum 25:653–676CrossRefGoogle Scholar
  127. Kulshreshtha G, Rathgeber B, Stratton G, Thomas N, Evans F, Critchley A, Hafting J, Prithiviraj B (2014) Feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poultry Sci 93:1–11CrossRefGoogle Scholar
  128. Kumar M, Kumari P, Trivedi N, Shukla MK, Gupta V, Reddy CRK, Jha B (2011) Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Saurashtra coast of India. J Appl Phycol 23:797–810CrossRefGoogle Scholar
  129. Kupfermann I (1975) Neurophysiology of learning. Annu Rev Psychol 26:367–391PubMedCrossRefGoogle Scholar
  130. Kwak CS, Lee MS, Lee HJ, Whang JY, Park SC (2010) Dietary source of vitamin B12 intake and vitamin B12 status in female elderly Koreans aged 85 and older living in rural area. Nutr Res Pract 4:229–234PubMedPubMedCentralCrossRefGoogle Scholar
  131. Kyriacou K, Parkington JE, Marais AD, Braun DR (2014) Nutrition, modernity and the archaeological record: coastal resources and nutrition among Middle Stone Age hunter-gatherers on the western Cape coast of South Africa. J Human Evol 77:64–73CrossRefGoogle Scholar
  132. Lauritzen L, Hansen HS, Jørgensen MH, Michaelsen KF (2001) The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 40:1–94PubMedCrossRefGoogle Scholar
  133. Laycock MV, Craigie JS (1977) The occurrence and seasonal variation of gigartinine and L-citrullinyl-L-arginine in Chondrus crispus Stackh. Can J Biochem 55:27–30PubMedCrossRefGoogle Scholar
  134. Laycock MN, Morgan KC, Craigie JS (1981) Physiological factors affecting the accumulation of L-citrullinyl-L-arginine in Chondrus crispus. Can J Bot 59:522–527CrossRefGoogle Scholar
  135. Leonard WR (2002) Food for thought: dietary change was a driving force in human evolution. Sci Am 287:106–115PubMedCrossRefGoogle Scholar
  136. Leonard WR, Robertson ML (1997) Comparative primate energetics and hominid evolution. Am J Phys Anthropol 102:265–281PubMedCrossRefGoogle Scholar
  137. Leonard WR, Snodgrass JJ, Robertson ML (2010) Evolutionary perspectives on fat ingestion and metabolism in humans. In: Fat detection: taste, texture, and post ingestive effects. Editors: Montmayeur JP, le Coutre J. CRC Press/Taylor & Francis, Boca Raton.Google Scholar
  138. Li M, Eastman CJ, Waite KV, Ma G, Zacharin MR, Topliss DJ, Harding PE, Walsh JP, Ward LC, Mortimer RH, Mackenzie EJ, Byth K, Doyle Z (2006) Are Australian children iodine deficient? Results of the Australian National Iodine Study. Med J Aust 184:165–169PubMedGoogle Scholar
  139. Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M (2009) Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 96:557–567PubMedCrossRefGoogle Scholar
  140. Lieberman DE (2011) The evolution of the human head. Harvard University Press, CambridgeGoogle Scholar
  141. Lieberman DE (2013) The story of the human body. Evolution, health, and disease. Pantheon, New YorkGoogle Scholar
  142. Lindorfer H, Krebs M, Kautzky-Willer A, Bancher-Todesca D, Sager M, Gessl A (2015) Iodine deficiency in pregnant women in Austria. Eur J Clin Nutr 69:349–354PubMedCrossRefGoogle Scholar
  143. Liu Z, Chopp M (2016) Astrocytes, therapeutic targets for neuroprotection and neurorestoration in ischemic stroke. Prog Neurobiol 144:103–120PubMedCrossRefGoogle Scholar
  144. Liu X, Zhang W, Liu T, Xiao H, Liang W, Xia W, Zhang J (2013) Perinatal supplementation with omega-3 polyunsaturated fatty acids improves sevoflurane-induced neurodegeneration and memory impairment in neonatal rats. PLoS One 8:e70645PubMedPubMedCentralCrossRefGoogle Scholar
  145. Liu J, Banskota AH, Critchley AT, Hafting J, Prithiviraj B (2015) Neuroprotective effects of the cultivated Chondrus crispus in a C. elegans model of Parkinson’s disease. Mar Drugs 13:2250–2266PubMedPubMedCentralCrossRefGoogle Scholar
  146. Lövblad KO, Ramelli G, Remonda L, Nirkko AC, Ozdoba C, Schroth G (1997) Retardation of myelination due to dietary vitamin B12 deficiency: cranial MRI findings. Pediatr Radiol 27:155–158PubMedCrossRefGoogle Scholar
  147. Luca F, Perry GH, Di Rienzo A (2010) Evolutionary adaptations to dietary changes. Annu Rev Nutr 30:291–314PubMedPubMedCentralCrossRefGoogle Scholar
  148. Luchtman DW, Song C (2013) Cognitive enhancement by omega-3 fatty acids from child-hood to old age: findings from animal and clinical studies. Neuropharmacol 64:550–565CrossRefGoogle Scholar
  149. Maberly SC, Raven JA, Johnston AM (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492PubMedCrossRefGoogle Scholar
  150. MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543PubMedCrossRefGoogle Scholar
  151. MacDonald RS (2000) The role of zinc in growth and cell proliferation. J Nutr 130:1500S–1508SPubMedGoogle Scholar
  152. Marean CW (2014) The origins and significance of coastal resource use in Africa and Western Eurasia. J Human Evol 77:17–40CrossRefGoogle Scholar
  153. Marques AH, O’Connor TG, Roth C, Susser E, Bjørke-Monsen A-L (2013) The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopment disorders. Front Neurosci 7:120. doi:10.3389/fnins.2013.00120 PubMedPubMedCentralCrossRefGoogle Scholar
  154. Martínez M, Mougan I (1998) Human brain phospholipids during normal development. J Neurochem 71:2528–2533PubMedCrossRefGoogle Scholar
  155. Mayer EA (2011) Gut feelings: the emerging biology of gut-brain communication. Nat Rev Neurosci 12:453–466PubMedCrossRefGoogle Scholar
  156. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236PubMedPubMedCentralCrossRefGoogle Scholar
  157. McKenzie IA, Ohayon D, Li H, de Faria JP, Emery B, Tohyama K, Richardson WD (2014) Motor skill learning requires active central myelination. Science 346:318–322PubMedCrossRefGoogle Scholar
  158. Meenakshi S, Umayaparvathi S, Saravanan R, Manivasagam T, Balasubramanian T (2016) Neuroprotective effect of fucoidan from Turbinaria decurrens in MPTP intoxicated Parkinsonic mice. Int J Biol Macromol 86:425–433PubMedCrossRefGoogle Scholar
  159. Menezes A, Artham S, Lavie CJ, Milani RV, O’Keefe J (2011) Erectile dysfunction and cardiovascular disease. Postgrad Med 123:7–16PubMedCrossRefGoogle Scholar
  160. Milton K (1987) Primate diets and gut morphology: implications for human evolution. In: Harris M, Ross EB (eds) Food and evolution: toward a theory of human food habits. Temple University Press, Philadelphia, pp 93–116Google Scholar
  161. Misheer N, Kindness A, Jonnalagadda SB (2006) Elemental distribution in seaweed, Gelidium abbottiorum along the KwaZulu-Natal coastline, South Africa. J Environ Sci Health A 41:1639–1653CrossRefGoogle Scholar
  162. Miyashita K, Mikami N, Hosokawa M (2013) Chemical and nutritional characteristics of brown seaweed lipids: a review. J Funct Foods 5:1507–1517CrossRefGoogle Scholar
  163. Modgil S, Lahiri DK, Sharma VL, Anand A (2014) Role of early life exposure and environment on neurodegeneration: implications on brain disorders. Trans Neurodegen 3:9CrossRefGoogle Scholar
  164. Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Tech 23:83–96CrossRefGoogle Scholar
  165. Mohibbullah M, Hannan MA, Choi JY, Bhuiyan MMH, Hong YK, Choi JS, Choi IS, Moon IS (2015) The edible marine alga Gracilariopsis chorda alleviates hypoxia/reoxygenation-induced oxidative stress in cultured hippocampal neurons. J Med Food 18:960–971PubMedPubMedCentralCrossRefGoogle Scholar
  166. Mohibbullah M, Bhuiyan MMH, Hannan MA, Getachew P, Hong YK, Choi JS, Choi IS (2016) The edible red alga Porphyra yezoensis promotes neuronal survival and cytoarchitecture in primary hippocampal neurons. Cell Mol Neurobiol 36:669–682PubMedCrossRefGoogle Scholar
  167. Moncayo R, Ortner K (2015) Multifactorial determinants of cognition—thyroid function is not the only one. BBA Clin 3:289–298PubMedPubMedCentralCrossRefGoogle Scholar
  168. Morell P, Quarles RH (1999) Characteristic composition of myelin. In: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD (eds)  Basic neurochemistry: molecular, cellular and medical aspects, 6th edn. Lippincott-Raven, PhiladelphiaGoogle Scholar
  169. Morris RGM (2013) NMDA receptors and memory encoding. Neuropharm 74:32–40CrossRefGoogle Scholar
  170. Mouritsen OG (2005) Life—as a matter of fat. The emerging science of lipidomics. Springer, Berlin, pp 1–276Google Scholar
  171. Mouritsen OG (2013) Seaweeds: edible, available & sustainable. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  172. Mouritsen OG (2016) Deliciousness of food and a proper balance in fatty acid composition as means to improve human health and regulate food intake. Flavour 5:1CrossRefGoogle Scholar
  173. Mouritsen OG, Crawford MA (eds) (2007) Poly-unsaturated fatty acids, neural function, and mental health. Biol Skr Dan Vid Selsk 56:1–87Google Scholar
  174. Myung CS, Shin HC, Bao HY, Yeo SJ, Lee BH, Kang JS (2005) Improvement of memory by dieckol and phlorofucofuroeckol in ethanol-treated mice: possible involvement of the inhibition of acetylcholinesterase. Arch Pharm Res 28:691–698PubMedCrossRefGoogle Scholar
  175. Nakamura E, Yokota H, Matsui T (2012) The in vitro digestibility and absorption of magnesium in some edible seaweeds. J Sci Food Agric 92:2305–2309PubMedCrossRefGoogle Scholar
  176. Navarrete A, van Schaik CP, Isler K (2011) Energetics and the evolution of human brain size. Nature 480:91–93PubMedCrossRefGoogle Scholar
  177. NIH (National Institutes of Health) (2016) Zinc Fact Sheet https://ods.od.nih.gov/factsheets/Zinc-HealthProfessional/. (Accesed December 23, 2016)
  178. Nils-Erik LS, Mervaala E, Karppanen H, Khauraja JA, Lewenstam A (2000) Magnesium an update on physiological, clinical and analytical aspects. Clinica Chim Acta 294:1–26CrossRefGoogle Scholar
  179. NINDS (National Institute of Neurological Disorders and Stroke) (2015) Brain basics: know your brain. www.ninds.nih.gov. (Accessed August 10, 2016)
  180. Nitschke U, Stengel DB (2015) A new HPLC method for the detection of iodine applied to natural samples of edible seaweeds and commercial seaweed food products. Food Chem 172:326–334PubMedCrossRefGoogle Scholar
  181. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462–465PubMedCrossRefGoogle Scholar
  182. NRC Food and Nutrition Board (1989) Recommended dietary allowances, 10th edn. National Academy Press, Washington DC, p 302Google Scholar
  183. Olesen J, Gustavsson A, Svensson M, Wittchen H-U, Jönsson B (2012) The economic cost of brain disorders in Europe. Eur J Neurol 19:155–162PubMedCrossRefGoogle Scholar
  184. Oriach CS, Robertson RC, Stanton C, Cryan JF, Dinan TG (2016) Food for thought: the role of nutrition in the microbiota-gut-brain axis. Clin Nutr Exper 6:25–38CrossRefGoogle Scholar
  185. Otten JJ, Hellwig JP, Meyers LD (2006) Dietary reference intakes: the essential guide to nutrient requirements. Institute of Medicine, National Academy Press, Washington, D.C.Google Scholar
  186. Paiva L, Lima E, Patarra RF, Neto AI, Baptista J (2014) Edible Azorean macroalgae as source of rich nutrients with impact on human health. Food Chem 164:128–135PubMedCrossRefGoogle Scholar
  187. Pangestuti R, Kim SK (2011) Neuroprotective effects of marine algae. Mar Drugs 9:803–818PubMedPubMedCentralCrossRefGoogle Scholar
  188. Pereira L (2011) A review of the nutrient composition of selected edible seaweeds. In: Pomin VH (ed) Seaweed:ecology, nutrient composition and medicinal uses. Nova Publishers Inc, New York, pp 15–47Google Scholar
  189. Prado EL, Dewey KG (2014) Nutrition and brain development in early life. Nutr Rev 72:267–284PubMedCrossRefGoogle Scholar
  190. Prasad AS (2013) Discovery of human zinc deficiency: its impact on human health and disease. Adv Nutr 4:176–190PubMedPubMedCentralCrossRefGoogle Scholar
  191. Preuss TM (2011) The human brain: rewired and running hot. Ann N Y Acad Sci 1225(S1):E182–E191PubMedPubMedCentralCrossRefGoogle Scholar
  192. Pu H, Guo Y, Zhang W, Huang L, Wang G, Liou AK, Zhang J, Zhang P, Leak RK, Wang Y, Chen J, Gao Y (2013) Omega-3 polyunsaturated fatty acid supplementation improves neurologic recovery and attenuates white matter injury after experimental traumatic brain injury. J Cereb Blood Flow Metab 33:1474–1484PubMedPubMedCentralCrossRefGoogle Scholar
  193. Rafiquzzaman SM, Kim EY, Lee JM, Mohibbullah M, Alam MB, Moon IS, Kim JM, Kong IS (2015) Anti-Alzheimers and anti-inflammatory activities of a glycoprotein purified from the edible brown alga Undaria pinnatifida. Food Res Int 77:118–124CrossRefGoogle Scholar
  194. Ramnani P, Chitarrari R, Tuohy K, Grant J, Hotchkiss S, Philp K, Campbell R, Gill C, Rowland I (2012) In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe 18:1–6PubMedCrossRefGoogle Scholar
  195. Raposo MFJ, Morais AMMB, Morais RMSC (2016) Emergent sources of prebiotics: seaweeds and microalgae. Mar Drugs 14(2):27CrossRefGoogle Scholar
  196. Ratana-arporn P, Chirapart A (2006) Nutritional evaluation of tropical green seaweeds Caulerpa lentillifera and Ulva reticulata. Kasetsart J Nat Sci 40(Suppl):75–83Google Scholar
  197. Rath CM, Alexandrov T, Higginbottom SK, Song J, Milla ME, Fischbach MA, Sonnenburg JL, Dorrestein PC (2012) Molecular analysis of model gut microbiotas by imaging mass spectrometry and nanodesorption electrospray ionization reveals dietary metabolite transformations. Anal Chem 84:9259–9267PubMedPubMedCentralCrossRefGoogle Scholar
  198. Rauma AL, Törrönen R, Hänninen O, Mykkänen H (1995) Vitamin B-12 status of long-term adherents of a strict uncooked vegan diet (“living food diet”) is compromised. J Nutr 125:2511–2515PubMedGoogle Scholar
  199. Reilly P, O’Doherty JV, Pierce KM, Callan JJ, O’Sullivan JT, Sweeney T (2008) The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2:1465–1473PubMedCrossRefGoogle Scholar
  200. Rilling JK (2014) Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn Sci 18:46–55PubMedCrossRefGoogle Scholar
  201. Rink L, Gabriel P (2000) Zinc and the immune system. Proc Nutr Soc 59:541–552PubMedCrossRefGoogle Scholar
  202. Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de los Reyes-Gavilán CG, Salazar N (2016) Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol 7:185PubMedPubMedCentralCrossRefGoogle Scholar
  203. Rohling EJ, Foster GL, Grant KM, Marino G, Roberts AP, Tamisiea ME, Williams F (2014) Sea-level and deep-sea-temperature variability over the past 5.3 million years. Nature 508:477–482PubMedCrossRefGoogle Scholar
  204. Rosenblatt DS, Whitehead VM (1999) Cobalamin and folate deficiency: acquired and hereditary disorders in children. Semin Hematol 36:19–34PubMedGoogle Scholar
  205. Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9:250–257PubMedCrossRefGoogle Scholar
  206. Roumeliotis N, Dix D, Lipson A (2012) Vitamin B12 deficiency in infants secondary to maternal causes. CMAJ 184:1593–1598PubMedPubMedCentralCrossRefGoogle Scholar
  207. Roy B, Trivedi R, Garg RK, Gupta PK, Tyagi R, Gupta RK (2015) Assessment of functional and structural damage in brain parenchyma in patients with vitamin B12 deficiency: a longitudinal perfusion and diffusion tensor imaging study. Magn Res Imag 33:537–543CrossRefGoogle Scholar
  208. Saher G, Brügger B, Lappe-Siefke C, Möbius W, Tozawa R, Wehr MC, Wieland F, Ishibashi S, Nave K-A (2005) High cholesterol level is essential for myelin membrane growth. Nature Neurosci 8:468–475PubMedGoogle Scholar
  209. Sakai T, Matsui M, Mikami A, Malkova L, Hamada Y, Tomonaga M, Suziki J, Tanaka M, Miyabe-Nishiwaki T, Makishima H, Nakatsukasa M, Matsuzawa T (2012) Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain. Proc R Soc B 280:20122398PubMedCrossRefGoogle Scholar
  210. Sandstead HH (1991) Zinc deficiency. A public health problem? Am J Dis Child 145:853–859PubMedCrossRefGoogle Scholar
  211. Sandstead HH, Frederickson CJ, Penland JG (2000) History of zinc as related to brain function. J Nutr 130:496S–502SPubMedGoogle Scholar
  212. Sansalone S, Leonardi R, Antonini G, Vitarelli A, Vespasiani G, Basic D, Morgia G, Cimino S, Russo GI (2014) Alga Ecklonia bicyclis, Tribulus terrestris, and glucosamine oligosaccharide improve erectile function, sexual quality of life, and ejaculation function in patients with moderate mild-moderate erectile dysfunction: a prospective, randomized, placebo-controlled, single-blinded study. Biomed Res Int:121396. doi:10.1155/2014/121396
  213. Schenker NM, Desgouttes AM, Semendeferi K (2005) Neural connectivity and cortical substrates of cognition in hominoids. J Human Evol 49:547–569CrossRefGoogle Scholar
  214. Schmid M, Guihéneuf F, Stengel DB (2014) Fatty acid contents and profiles of 16 macroalgae collected from the Irish Coast at two seasons. J Appl Phycol 26:451–463CrossRefGoogle Scholar
  215. Schoenemann PT (2006) Evolution of the size and functional areas of the human brain. Annu Rev Anthropol 35:379–406CrossRefGoogle Scholar
  216. Scholz J, Klein MC, Behrens TEJ, Johansen-Berg H (2009) Training induces changes in white-matter architecture. Nature Neurosci 12:1370–1371PubMedPubMedCentralCrossRefGoogle Scholar
  217. Scott C, Planavsky NJ, Dupont CL, Kendall B, Gill BC, Robbins LJ, Husband KF, Arnold GL, Wing BA, Poulton SW, Bekker A, Anbar AD, Konhauser KO, Lyons TW (2013) Bioavailability of zinc in marine systems through time. Nat Geosci 6:125–128CrossRefGoogle Scholar
  218. Sensi SL, Paoletti P, Koh J-Y, Aizenman E, Bush AI, Hershfinkel M (2011) The neurophysiology and pathology of brain zinc. J Neurosci 31:16076–16085PubMedPubMedCentralCrossRefGoogle Scholar
  219. Shapiro M (2016) Gut microbiotas and host evolution: scaling up endosymbiosis. Trends Ecol Evol 31:539–549CrossRefGoogle Scholar
  220. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688CrossRefGoogle Scholar
  221. Sistiaga A, Wrangham R, Rothman JM, Summons RE (2015) New insights into the evolution of the human diet from faecal biomarker analysis in wild chimpanzee and gorilla faeces. PLoS One 10:e0128931PubMedPubMedCentralCrossRefGoogle Scholar
  222. Slutsky I, Abumaria N, Wu L-J, Huang C, Zhang L, Li B, Zhao X, Govindarajan A, Zhao M-G, Zhuo M, Tonegawa S, Liu G (2010) Enhancement of learning and memory by elevating brain magnesium. Neuron 65:165–177PubMedCrossRefGoogle Scholar
  223. Smaers JB, Steele J, Case CR, Cowper A, Amunts K, Zilles K (2011) Primate prefrontal cortex evolution: human brains are the extreme of a lateralized ape trend. Brain Behav Evol 77:67–78PubMedCrossRefGoogle Scholar
  224. Smith PM, Jeffery ND (2006) Histological and ultrastructural analysis of white matter damage after naturally-occurring spinal cord injury. Brain Pathol 16:99–109PubMedCrossRefGoogle Scholar
  225. Smyth PPA, Burns R, Huang RJ, Hoffman T, Mullan K, Graham U, Seitz K, Platt U, O’Dowd C (2011) Does iodine gas released from seaweed contribute to dietary iodine intake? Environ Geochem Health 33:389–387PubMedCrossRefGoogle Scholar
  226. Sponheimer M, Lee-Thorp JA (1999) Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283:368–370PubMedCrossRefGoogle Scholar
  227. Sponheimer M, Alemseged Z, Cerling TE, Grine FE, Kimbel WH, Leakey MG, Lee-Thorp JA, Manthi FK, Reed KE, Wood BA, Wynn JG (2013) Isotopic evidence of early hominin diets. PNAS 110:10513–10518PubMedCentralCrossRefGoogle Scholar
  228. Stabler SP (2013) Vitamin B12 deficiency. N Engl J Med 368:149–160PubMedCrossRefGoogle Scholar
  229. Stengel D, Macken A, Morrison L, Morley N (2004) Zinc concentrations in marine macroalgae and a lichen from western Ireland in relation to phylogenetic grouping, habitat and morphology. Mar Poll Bull 48:902–909CrossRefGoogle Scholar
  230. Stewart KM (2014) Environmental change and hominin exploitation of C4-based resources in wetland/savanna mosaics. J Human Evol 77:1–16CrossRefGoogle Scholar
  231. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, Kubo C, Koga Y (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558:263–275PubMedPubMedCentralCrossRefGoogle Scholar
  232. Suganthy N, Pandian SK, Devi KP (2010) Neuroprotective effect of seaweeds inhabiting South Indian coastal area (Hare Island, Gulf of Mannar Marine Biosphere Reserve): Cholinesterase inhibitory effect of Hypnea valentiae and Ulva reticulata. Neurosci Lett 468:216–219Google Scholar
  233. Syad AN, Shunmugiah KP, Kasi PD (2012) Assessment of anticholinesterase activity of Gelidiella acerosa: implications for its therapeutic potential against Alzheimer’s disease. Evid Based Compl Alt Med. doi:10.1155/2012/497242 Google Scholar
  234. Syad AN, Rajamohamed BS, Shunmugaiah KP, Kasi PD (2016) Neuroprotective effect of the marine macroalga Gelidiella acerosa: identification of active compounds through bioactivity-guided fractionation. Pharm Biol 54:2073–2081PubMedCrossRefGoogle Scholar
  235. Tan H, O’Toole PW (2015) Impact of diet on the human intestinal microbiota. Curr Opin Food Sci 2:71–77CrossRefGoogle Scholar
  236. Teas J, Pino S, Critchley A, Braverman LE (2004) Variability of iodine content in common commercially available edible seaweeds. Thyroid 14:836–841PubMedCrossRefGoogle Scholar
  237. Teffer K, Semendeferi K (2012) Chapter 9—human prefrontal cortex: evolution, development, and pathology. Prog Brain Res 195:191–218PubMedCrossRefGoogle Scholar
  238. Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2:93PubMedPubMedCentralCrossRefGoogle Scholar
  239. Tirtawijaya G, Mohibbullah M, Meinita MDN, Moon IS, Hong YK (2016) The ethanol extract of the rhodophyte Kappaphycus alvarezii promotes neurite outgrowth in hippocampal neurons. J Appl Phycol 28:2515–2522CrossRefGoogle Scholar
  240. Toque HA, Caldwell RW (2014) New approaches to the design and discovery of therapies to prevent erectile dysfunction. Expert Opin Drug Discov 9:1447–1469PubMedCrossRefGoogle Scholar
  241. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405–496PubMedPubMedCentralCrossRefGoogle Scholar
  242. Tuzun F, Kumral A, Dilek M, Ozbal S, Ergur B, Yesilirmak DC, Duman N, Yilmaz O, Ozkan H (2012) Maternal omega-3 fatty acid supplementation protects against lipopolysaccharide-induced white matter injury in the neonatal brain. J Mater Fetal Neonat Med 25:849–854CrossRefGoogle Scholar
  243. Uauy R, Mena P, Rojas C (2000) Essential fatty acids in early life: structural and functional role. Proc Nutr Soc 59:3–15PubMedCrossRefGoogle Scholar
  244. USDA, United States Department of Agriculture (2016) Food and nutrition information center. https://fnic.nal.usda.gov/food-composition (Accessed August 10, 2016)
  245. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP (2010) Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2:53–66PubMedPubMedCentralCrossRefGoogle Scholar
  246. Vanderpump MPJ, Lazarus JH, Smyth PP, Laurberg P, Holder RL, Boelaert K, Franklyn JA (2011) Iodine status of UK schoolgirls: a cross-sectional survey. Lancet 377:2007–2012PubMedCrossRefGoogle Scholar
  247. von Schenck U, Bender-Götze C, Koletzko B (1997) Persistence of neurological damage induced by dietary vitamin B-12 deficiency in infancy. Arch Dis Child 77:137–139CrossRefGoogle Scholar
  248. Wang Y, Han F, Hu B, Li J, Yu W (2006) In vivo prebiotic properties of alginate oligosaccharides prepared through enzymatic hydrolysis of alginate. Nutr Res 26:597–603CrossRefGoogle Scholar
  249. Ward RE, Huang W, Curran OE, Priestley JV, Michael-Titus AT (2010) Docosahexaenoic acid prevents white matter damage after spinal cord injury. J Neurotr 27:1769–1780CrossRefGoogle Scholar
  250. Watanabe F (2007) Vitamin B12 sources and bioavailability. Exper Biol Med 232:1266–1274CrossRefGoogle Scholar
  251. Watanabe F, Yabuta Y, Bito T, Teng F (2014) Vitamin B12-containing plant food sources for vegetarians. Nutrients 6:1861–1873PubMedPubMedCentralCrossRefGoogle Scholar
  252. Watkins PA, Moser AB, Toomer CB, Steinberg SJ, Moser HW, Karaman MW, Ramaswamy K, Siegmund KD, Lee DR, Ely JJ, Ryder OA, Hacia JG (2010) Identification of differences in human and great ape phytanic acid metabolism that could influence gene expression profiles and physiological functions. BMC Physiol 10:19PubMedPubMedCentralCrossRefGoogle Scholar
  253. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2016) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol doi:10.1007/s10811-016-0974-5
  254. Wessells KR, Brown KH (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One 7:e50568PubMedPubMedCentralCrossRefGoogle Scholar
  255. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci 95:6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  256. WHO (World Health Organization) (2002) The world health report. Chapter 4: reducing risks, promoting healthy life. http://www.who.int/whr/2002/chapter4/en/index3.html (Accessed August 10, 2016)
  257. WHO (World Health Organization) (2007) Iodine deficiency in Europe: a continuing public health problem. http://www.who.int/nutrition/publications/VMNIS_Iodine_deficiency_in_Europe.pdf (Accessed August 10, 2016)
  258. Wiggins RC (1982) Myelin development and nutritional insufficiency. Brain Res 257:151–175PubMedCrossRefGoogle Scholar
  259. Wrangham RW (2009) Catching fire: how cooking made us human. Basic Books, New YorkGoogle Scholar
  260. Wrangham RW, Conklin-Brittain N (2003) Cooking as a biological trait. Comp Biochim Physiol A 136:35–46CrossRefGoogle Scholar
  261. Wynn JG, Sponheimer M, Kimbel WH, Alemseged Z, Reed K, Bedaso ZK, Wilson JN (2013) Diet of Australopithecus afarensis from the Pliocene Hadar Formation, Ethiopia. PNAS 110:10495–10500PubMedPubMedCentralCrossRefGoogle Scholar
  262. Xu X, Wang Z, Zhang X (2015) The human microbiota associated with overall health. Crit Revnn 35:129–140Google Scholar
  263. Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, Nagler CR, Ismagilov RF, Mazmanian SK, Hsiao EY (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276PubMedPubMedCentralCrossRefGoogle Scholar
  264. Yehuda S, Carasso RL (1993) Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified α-linolenic and linoleic acids: determination of the optimal n3-to-n6 ratio. PNAS 90:10345–10349PubMedPubMedCentralCrossRefGoogle Scholar
  265. Yong YS, Yong WTL, Ng SE, Anton A, Yassir S (2015) Chemical composition of farmed and micropropagated Kappaphycus alvarezii (Rhodophyta, Gigartinales), a commercially important seaweed in Malaysia. J Appl Phycol 27:1271–1275CrossRefGoogle Scholar
  266. Youdim KA, Martin A, Joseph JA (2000) Essential fatty acids and the brain: possible health implications. Int J Dev Neurosci 18:383–399PubMedCrossRefGoogle Scholar
  267. Zaporozhets TS, Besednova NN, Kuznetsova TA, Zvyagintseva TN, Makarenkova ID, Kryzhanovsky SP, Melnikov VG (2014) The prebiotic potential of polysaccharides and extracts of seaweeds. Russ J Mar Biol 40:1–9CrossRefGoogle Scholar
  268. Zhao D, Zheng L, Qi L, Wang S, Guan L, Xia Y, Cai J (2016) Structural features and potent antidepressant effects of total sterols and β-sitosterol extracted from Sargassum horneri. Mar Drugs 14:123PubMedCentralCrossRefGoogle Scholar
  269. Zimmermann MB (2009) Iodine deficiency. Endocr Rev 30:376–408PubMedCrossRefGoogle Scholar
  270. Zimmermann MB, Connolly K, Bozo M, Bridson J, Rohner F, Grimci L (2006) Iodine supplementation improves cognition in iodine-deficient schoolchildren in Albania: a randomized, controlled, double-blind study. Am J Clin Nutr 83:108–114PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • M. Lynn Cornish
    • 1
  • Alan T. Critchley
    • 2
  • Ole G. Mouritsen
    • 3
  1. 1.J.S. Craigie Research CentreCornwallis ParkCanada
  2. 2.ParadiseCanada
  3. 3.MEMPHYS—Center for Biomembrane Physics, Taste for Life—Danish Center for Taste, Department of Physics, Chemistry and PharmacyUniversity of Southern DenmarkOdense MDenmark

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